Protein-mediated fusion of two membranes into one is an important stage of enveloped virus entry into host cells. The baculovirus fusogenic activity depends on the low pH conformation of trimeric gp64. We investigated whether monomers, trimers and/or higher order oligomers are functionally involved in gp64 fusion machine. Dithiothreitol (DTT) reduction of intersubunit disulfides in gp64 trimers caused their destabilization to dimers and monomers, and, in parallel, reversibly inhibited gp64-mediated fusion. Thus, stable gp64 trimers, rather than independent monomers, drive fusion. To merge the membranes, gp64 trimers assemble into large (greater than 2 MDa), short-lived gp64 complexes. These complexes were stabilized by cell-surface cross-linking and characterized by glycerol density gradient ultracentrifugation. DTT-destabilized trimers failed to form multimeric complexes indicating that the basic structural unit of the complexes is stable gp64 trimer. Formation of these complexes correlated with fusion in timing, and was dependent on (i) low pH application and (ii) cell contacts, suggesting that such multimeric complexes represent a fusion machine. To elucidate the coupling between protein refolding and assembly and membrane rearrangements, we theoretically analyzed fusion mediated by the best characterized fusion protein, influenza hemagglutinin, HA. We propose that the extension of the central coiled coil of HA pulls fusion peptides inserted into the HA-expressing membrane and bends the membrane around the HA trimer into a saddle-like shape. Elastic energy drives self-assembly of these HA-containing membrane elements in the membrane into a ring-like complex and causes the bulging of this membrane into a dimple growing towards the bound target membrane. Bending stresses in the lipidic top of the dimple facilitate membrane fusion. The mechanism of protein-driven membrane rearrangements studied here for viral fusion may be universal.